We have extended our technology for studying macromolecular structure in solution under weakly aligning conditions. New developments focus on the accurate measurement of dipolar interactions between protons. We have demonstrated that under favorable conditions, such direct interactions are observable over distances of up to 12 ?, without requiring special isotopic enrichment. The 1H-1H dipolar interaction depends on both the internuclear distance and on the orientation of the internuclear vector relative to the alignment frame of the molecule, and thereby constitutes a direct complement to the widely used 1H-1H NOE interaction, which depends only on the distance. The combination of 1H-1H dipolar interactions and 1H-13C couplings was shown to be sufficient to accurately define the solution structure of a DNA oligomer, but also showed that in particular the deoxyribose units of pyrimidine nucleotides were not compatible with a single, static conformation. They are, however, in agreement with a model where the sugar rapidly switches between a C2?-endo conformer (the dominant form), and a minor C3?-endo form. Our newly developed experiments permit the accurate measurement of an unprecedented number of dipolar couplings per structural unit (ribose, deoxyribose, or amino acid) and thereby provides a new avenue to explore the degree of alignment each unit experiences individually, thereby providing direct information on the degree of mobility, or lack thereof, of such units relative to the overall frame of the macromolecule. Previous work by others has explored the issue of intramolecular dynamics in nucleic acids on the basis of the observed degree of magnetic alignment, resulting from magnetic susceptibility anisotropy, and the actually observed alignment. Frequently, this led to conclusions that very large amplitude internal dynamics and hinge motions were present in nucleic acids. We have re-analyzed the intrinsic magnetic susceptibility of nucleic acids bases by both quantum-computational and experimental methods and find considerably smaller values than were commonly used by others. With our new base susceptibility values, the amplitude of domain motions in nucleic acids is of considerably smaller amplitude than concluded previously. This finding is of direct relevance for understanding the thermodynamic components in protein-nucleic acid recognition.